Macroalgae exhibit diverse responses to human disturbances on coral reefs.

Scientists and managers rely on indicator taxa such as coral and macroalgal cover to evaluate the effects of human disturbance on coral reefs, often assuming a universally positive relationship between local human disturbance and macroalgae. Despite evidence that macroalgae respond to local stressors in diverse ways, there have been few efforts to evaluate relationships between specific macroalgae taxa and local human-driven disturbance. Using genus-level monitoring data from 1205 sites in the Indian and Pacific Oceans, we assess whether macroalgae percent cover correlates with local human disturbance while accounting for factors that could obscure or confound relationships. Assessing macroalgae at genus level revealed that no genera were positively correlated with all human disturbance metrics. Instead, we found relationships between the division or genera of algae and specific human disturbances that were not detectable when pooling taxa into a single functional category, which is common to many analyses. The convention to use percent cover of macroalgae as an indication of local human disturbance therefore likely obscures signatures of local anthropogenic threats to reefs. Our limited understanding of relationships between human disturbance, macroalgae taxa, and their responses to human disturbances impedes the ability to diagnose and respond appropriately to these threats.

Effects of human footprint and biophysical factors on the body-size structure of fished marine species.

Marine fisheries in coastal ecosystems in many areas of the world have historically removed large-bodied individuals, potentially impairing ecosystem functioning and the long-term sustainability of fish populations. Reporting on size-based indicators that link to food-web structure can contribute to ecosystem-based management, but the application of these indicators over large (cross-ecosystem) geographical scales has been limited to either fisheries-dependent catch data or diver-based methods restricted to shallow waters (<20 m) that can misrepresent the abundance of large-bodied fished species. We obtained data on the body-size structure of 82 recreationally or commercially targeted marine demersal teleosts from 2904 deployments of baited remote underwater stereo-video (stereo-BRUV). Sampling was at up to 50 m depth and covered approximately 10,000 km of the continental shelf of Australia. Seascape relief, water depth, and human gravity (i.e., a proxy of human impacts) were the strongest predictors of the probability of occurrence of large fishes and the abundance of fishes above the minimum legal size of capture. No-take marine reserves had a positive effect on the abundance of fishes above legal size, although the effect varied across species groups. In contrast, sublegal fishes were best predicted by gradients in sea surface temperature (mean and variance). In areas of low human impact, large fishes were about three times more likely to be encountered and fishes of legal size were approximately five times more abundant. For conspicuous species groups with contrasting habitat, environmental, and biogeographic affinities, abundance of legal-size fishes typically declined as human impact increased. Our large-scale quantitative analyses highlight the combined importance of seascape complexity, regions with low human footprint, and no-take marine reserves in protecting large-bodied fishes across a broad range of species and ecosystem configurations.

Las pesquerías marinas de los ecosistemas costeros en muchas áreas del mundo históricamente han removido a individuos de gran tamaño, potencialmente perjudicando el funcionamiento ambiental y la sostenibilidad a largo plazo de las poblaciones de peces. Los reportes sobre los indicadores basados en el tamaño que se vinculan con la estructura de la red alimenticia pueden contribuir al manejo basado en el ecosistema, aunque la aplicación de estos indicadores a grandes (inter-ecosistemas) escalas geográficas ha estado limitada a datos de captura dependientes de las pesquerías o métodos basados en el buceo restringidos a aguas someras (<20 m), lo cual puede representar erróneamente la abundancia de peces de gran tamaño capturados para la pesca. Obtuvimos los datos de la estructura del tamaño corporal de 82 teleósteos marinos demersales focalizados por razones recreativas o comerciales tomados de 2,904 despliegues de video estéreo subacuático remoto con cebo (stereo-BRUV, en inglés). El muestreo se realizó hasta los 50 metros de profundidad y abarcó aproximadamente 10,000 km del talud continental de Australia. El relieve marino, la profundidad del agua y la gravedad humana (es decir, un indicador de los impactos humanos) fueron los pronosticadores más sólidos de la probabilidad de incidencia de los peces de gran tamaño y de la abundancia de peces por encima del tamaño legal mínimo de captura. Las reservas marinas de protección total tienen un efecto positivo sobre la abundancia de los peces que están por encima del tamaño legal, aunque el efecto varió según el grupo de especies. Como contraste, los peces de tamaño sublegal fueron pronosticados de mejor manera usando gradientes de la temperatura de la superficie marina (media y varianza). En las áreas con un impacto humano reducido, los peces de gran tamaño corporal tenían hasta tres veces mayor probabilidad de aparecer y los peces de tamaño legal eran aproximadamente cinco veces más abundantes. Para los grupos de especies conspicuas con afinidades contrastantes de hábitat, ambiente y biogeografía, la abundancia de peces de tamaño legal normalmente declinó conforme aumentó el impacto humano. Nuestros análisis cuantitativos a gran escala resaltan la importancia conjunta que tienen la complejidad marina, las regiones con una huella humana reducida y las reservas marinas de protección total para la protección de los peces de gran tamaño corporal en una extensa gama de especies y configuraciones ecosistémicas. Efectos de la Huella Humana y los Factores Biofísicos sobre la Estructura del Tamaño Corporal de Especies Marinas Capturadas para la Pesca.

Increased connectivity and depth improve the effectiveness of marine reserves.

Marine reserves are a key tool for the conservation of marine biodiversity, yet only ~2.5% of the world's oceans are protected. The integration of marine reserves into connected networks representing all habitats has been encouraged by international agreements, yet the benefits of this design has not been tested empirically. Australia has one of the largest systems of marine reserves, providing a rare opportunity to assess how connectivity influences conservation success. An Australia-wide dataset was collected using baited remote underwater video systems deployed across a depth range from 0 to 100 m to assess the effectiveness of marine reserves for protecting teleosts subject to commercial and recreational fishing. A meta-analytical comparison of 73 fished species within 91 marine reserves found that, on average, marine reserves had 28% greater abundance and 53% greater biomass of fished species compared to adjacent areas open to fishing. However, benefits of protection were not observed across all reserves (heterogeneity), so full subsets generalized additive modelling was used to consider factors that influence marine reserve effectiveness, including distance-based and ecological metrics of connectivity among reserves. Our results suggest that increased connectivity and depth improve the aforementioned marine reserve benefits and that these factors should be considered to optimize such benefits over time. We provide important guidance on factors to consider when implementing marine reserves for the purpose of increasing the abundance and size of fished species, given the expected increase in coverage globally. We show that marine reserves that are highly protected (no-take) and designed to optimize connectivity, size and depth range can provide an effective conservation strategy for fished species in temperate and tropical waters within an overarching marine biodiversity conservation framework.

Assessing National Biodiversity Trends for Rocky and Coral Reefs through the Integration of Citizen Science and Scientific Monitoring Programs.

Reporting progress against targets for international biodiversity agreements is hindered by a shortage of suitable biodiversity data. We describe a cost-effective system involving Reef Life Survey citizen scientists in the systematic collection of quantitative data covering multiple phyla that can underpin numerous marine biodiversity indicators at high spatial and temporal resolution. We then summarize the findings of a continental- and decadal-scale State of the Environment assessment for rocky and coral reefs based on indicators of ecosystem state relating to fishing, ocean warming, and invasive species and describing the distribution of threatened species. Fishing impacts are widespread, whereas substantial warming-related change affected some regions between 2005 and 2015. Invasive species are concentrated near harbors in southeastern Australia, and the threatened-species index is highest for the Great Australian Bight and Tasman Sea. Our approach can be applied globally to improve reporting against biodiversity targets and enhance public and policymakers' understanding of marine biodiversity trends.

Corrigendum: Assessing National Biodiversity Trends for Rocky and Coral Reefs through the Integration of Citizen Science and Scientific Monitoring Programs.

[This corrects the article DOI: 10.1093/biosci/biw180.].

Influence of nursery microhabitats on the future abundance of a coral reef fish.

Species habitat associations are often complex, making it difficult to assess their influence on populations. Among coral reef fishes, habitat requirements vary among species and with ontogeny, but the relative importance of nursery and adult-preferred habitats on future abundances remain unclear. Moreover, adult populations may be influenced by recruitment of juveniles and assessments of habitat importance should consider relative effects of juvenile abundance. We conducted surveys across 16 sites and 200 km of reef to identify the microhabitat preferences of juveniles, sub-adults and adults of the damselfish Pomacentrus moluccensis Microhabitat preferences at different life-history stages were then combined with 6 years of juvenile abundance and microhabitat availability data to show that the availability of preferred juvenile microhabitat (corymbose corals) at the time of settlement was a strong predictor of future sub-adult and adult abundance. However, the influence of nursery microhabitats on future population size differed spatially and at some locations abundance of juveniles and adult microhabitat (branching corals) were better predictors of local populations. Our results demonstrate that while juvenile microhabitats are important nurseries, the abundance of coral-dependent fishes is not solely dependent on these microhabitats, especially when microhabitats are readily available or following large influxes of juveniles.

Can juvenile supply predict future abundance of large-bodied reef fishes?

The extent to which juvenile abundance can predict future populations of lethrinids at Ningaloo Reef was assessed using size frequency data collected over 13 consecutive years. Annual abundance of juvenile lethrinids (<5 cm TL) was highest in northern Ningaloo during La Niña years, when seawater is warmer and oceanic currents stronger. Juvenile lethrinid abundance explained 35% of the variance in 1-2 year-old Lethrinus nebulosus abundance the following year, a steeper relationship in the north suggesting greater survival of juveniles. Juvenile lethrinid abundance was also positively correlated to abundance of 1-2 year-old L. atkinsoni in the southern region of Ningaloo. Abundance of juvenile lethrinids were however poor predictors of L. nebulosus and L. atkinsoni older than 2 years of age. Post settlement processes likely weaken the link between juvenile supply and abundance of lethrinids >2 years old making it difficult to accurately quantify the overall size of future lethrinid populations.

Tracking widespread climate-driven change on temperate and tropical reefs.

Warming seas, marine heatwaves, and habitat degradation are increasingly widespread phenomena affecting marine biodiversity, yet our understanding of their broader impacts is largely derived from collective insights from independent localized studies. Insufficient systematic broadscale monitoring limits our understanding of the true extent of these impacts and our capacity to track these at scales relevant to national policies and international agreements. Using an extensive time series of co-located reef fish community structure and habitat data spanning 12 years and the entire Australian continent, we found that reef fish community responses to changing temperatures and habitats are dynamic and widespread but regionally patchy. Shifts in composition and abundance of the fish community often occurred within 2 years of environmental or habitat change, although the relative importance of these two mechanisms of climate impact tended to differ between tropical and temperate zones. The clearest of these changes on temperate and subtropical reefs were temperature related, with responses measured by the reef fish thermal index indicating reshuffling according to the thermal affinities of species present. On low latitude coral reefs, the community generalization index indicated shifting dominance of habitat generalist fishes through time, concurrent with changing coral cover. Our results emphasize the importance of maintaining local ecological detail when scaling up datasets to inform national policies and global biodiversity targets. Scaled-up ecological monitoring is needed to discriminate among increasingly diverse drivers of large-scale biodiversity change and better connect presently disjointed systems of biodiversity observation, indicator research, and governance.

Influence of prey body characteristics and performance on predator selection.

At the time of settlement to the reef environment, coral reef fishes differ in a number of characteristics that may influence their survival during a predatory encounter. This study investigated the selective nature of predation by both a multi-species predator pool, and a single common predator (Pseudochromis fuscus), on the reef fish, Pomacentrus amboinensis. The study focused on the early post-settlement period of P. amboinensis, when mortality, and hence selection, is known to be highest. Correlations between nine different measures of body condition/performance were examined at the time of settlement, in order to elucidate the relationships between different traits. Single-predator (P. fuscus) choice trials were conducted in 57.4-l aquaria with respect to three different prey characteristics [standard length (SL), body weight and burst swimming speed], whilst multi-species trials were conducted on open patch reefs, manipulating prey body weight only. Relationships between the nine measures of condition/performance were generally poor, with the strongest correlations occurring between the morphological measures and within the performance measures. During aquaria trials, P. fuscus was found to be selective with respect to prey SL only, with larger individuals being selected significantly more often. Multi-species predator communities, however, were selective with respect to prey body weight, with heavier individuals being selected significantly more often than their lighter counterparts. Our results suggest that under controlled conditions, body length may be the most important prey characteristic influencing prey survival during predatory encounters with P. fuscus. In such cases, larger prey size may actually be a distinct disadvantage to survival. However, these relationships appear to be more complex under natural conditions, where the expression of prey characteristics, the selectivity fields of a number of different predators, their relative abundance, and the action of external environmental characteristics, may all influence which individuals survive.

Climatic forcing and larval dispersal capabilities shape the replenishment of fishes and their habitat-forming biota on a tropical coral reef.

Fluctuations in marine populations often relate to the supply of recruits by oceanic currents. Variation in these currents is typically driven by large-scale changes in climate, in particular ENSO (El Nino Southern Oscillation). The dependence on large-scale climatic changes may, however, be modified by early life history traits of marine taxa. Based on eight years of annual surveys, along 150 km of coastline, we examined how ENSO influenced abundance of juvenile fish, coral spat, and canopy-forming macroalgae. We then investigated what traits make populations of some fish families more reliant on the ENSO relationship than others. Abundance of juvenile fish and coral recruits was generally positively correlated with the Southern Oscillation Index (SOI), higher densities recorded during La Niña years, when the ENSO-influenced Leeuwin Current is stronger and sea surface temperature higher. The relationship is typically positive and stronger among fish families with shorter pelagic larval durations and stronger swimming abilities. The relationship is also stronger at sites on the coral back reef, although the strongest of all relationships were among the lethrinids (r = .9), siganids (r = .9), and mullids (r = .8), which recruit to macroalgal meadows in the lagoon. ENSO effects on habitat seem to moderate SOI-juvenile abundance relationship. Macroalgal canopies are higher during La Niña years, providing more favorable habitat for juvenile fish and strengthening the SOI effect on juvenile abundance. Conversely, loss of coral following a La Niña-related heat wave may have compromised postsettlement survival of coral dependent species, weakening the influence of SOI on their abundance. This assessment of ENSO effects on tropical fish and habitat-forming biota and how it is mediated by functional ecology improves our ability to predict and manage changes in the replenishment of marine populations.

Human Disruption of Coral Reef Trophic Structure.

The distribution of biomass among trophic levels provides a theoretical basis for understanding energy flow and the hierarchical structure of animal communities. In the absence of energy subsidies [1], bottom-heavy trophic pyramids are expected to predominate, based on energy transfer efficiency [2] and empirical evidence from multiple ecosystems [3]. However, the predicted pyramid of biomass distribution among trophic levels may be disrupted through trophic replacement by alternative organisms in the ecosystem, trophic cascades, and humans preferentially impacting specific trophic levels [4-6]. Using empirical data spanning >250 coral reefs, we show how trophic pyramid shape varies given human-mediated gradients along two orders of magnitude in reef fish biomass. Mean trophic level of the assemblage increased modestly with decreasing biomass, contrary to predictions of fishing down the food web [7]. The mean trophic level pattern is explained by trophic replacement of herbivorous fish by sea urchins at low biomass and the accumulation of slow-growing, large-bodied, herbivorous fish at high biomass. Further, at high biomass, particularly where fishers are not selectively removing higher trophic level individuals, a concave trophic distribution emerges. The concave trophic distribution implies a more direct link between lower and upper trophic levels, which may confer greater energy efficiency. This trophic distribution emerges when community biomass exceeds ∼650 kg/ha, suggesting that fisheries for upper trophic level species will only be supported under lightly fished scenarios.

Climate-driven regime shift of a temperate marine ecosystem.

Ecosystem reconfigurations arising from climate-driven changes in species distributions are expected to have profound ecological, social, and economic implications. Here we reveal a rapid climate-driven regime shift of Australian temperate reef communities, which lost their defining kelp forests and became dominated by persistent seaweed turfs. After decades of ocean warming, extreme marine heat waves forced a 100-kilometer range contraction of extensive kelp forests and saw temperate species replaced by seaweeds, invertebrates, corals, and fishes characteristic of subtropical and tropical waters. This community-wide tropicalization fundamentally altered key ecological processes, suppressing the recovery of kelp forests.

Habitat Selectivity and Reliance on Live Corals for Indo-Pacific Hawkfishes (Family: Cirrhitidae).

Hawkfishes (family: Cirrhitidae) are small conspicuous reef predators that commonly perch on, or shelter within, the branches of coral colonies. This study examined habitat associations of hawkfishes, and explicitly tested whether hawkfishes associate with specific types of live coral. Live coral use and habitat selectivity of hawkfishes was explored at six locations from Chagos in the central Indian Ocean extending east to Fiji in the Pacific Ocean. A total of 529 hawkfishes from seven species were recorded across all locations with 63% of individuals observed perching on, or sheltering within, live coral colonies. Five species (all except Cirrhitus pinnulatus and Cirrhitichthys oxycephalus) associated with live coral habitats. Cirrhitichthys falco selected for species of Pocillopora while Paracirrhites arcatus and P. forsteri selected for both Pocillopora and Acropora, revealing that these habitats are used disproportionately more than expected based on the local cover of these coral genera. Habitat selection was consistent across geographic locations, and species of Pocillopora were the most frequently used and most consistently selected even though this coral genus never comprised more than 6% of the total coral cover at any of the locations. Across locations, Paracirrhites arcatus and P. forsteri were the most abundant species and variation in their abundance corresponded with local patterns of live coral cover and abundance of Pocilloporid corals, respectively. These findings demonstrate the link between small predatory fishes and live coral habitats adding to the growing body of literature highlighting that live corals (especially erect branching corals) are critically important for sustaining high abundance and diversity of fishes on coral reefs.

Relative and combined effects of habitat and fishing on reef fish communities across a limited fishing gradient at Ningaloo.

Habitat degradation and fishing are major drivers of temporal and spatial changes in fish communities. The independent effects of these drivers are well documented, but the relative importance and interaction between fishing and habitat shifts is poorly understood, particularly in complex systems such as coral reefs. To assess the combined and relative effects of fishing and habitat we examined the composition of fish communities on patch reefs across a gradient of high to low structural complexity in fished and unfished areas of the Ningaloo Marine Park, Western Australia. Biomass and species richness of fish were positively correlated with structural complexity of reefs and negatively related to macroalgal cover. Total abundance of fish was also positively related to structural complexity, however this relationship was stronger on fished reefs than those where fishing is prohibited. The interaction between habitat condition and fishing pressure is primarily due to the high abundance of small bodied planktivorous fish on fished reefs. However, the influence of management zones on the abundance and biomass of predators and target species is small, implying spatial differences in fishing pressure are low and unlikely to be driving this interaction. Our results emphasise the importance of habitat in structuring reef fish communities on coral reefs especially when gradients in fishing pressure are low. The influence of fishing effort on this relationship may however become more important as fishing pressure increases.

Unprecedented mass bleaching and loss of coral across 12° of latitude in Western Australia in 2010-11.

BACKGROUND: Globally, coral bleaching has been responsible for a significant decline in both coral cover and diversity over the past two decades. During the summer of 2010-11, anomalous large-scale ocean warming induced unprecedented levels of coral bleaching accompanied by substantial storminess across more than 12° of latitude and 1200 kilometers of coastline in Western Australia (WA). METHODOLOGY/PRINCIPAL FINDINGS: Extreme La-Niña conditions caused extensive warming of waters and drove considerable storminess and cyclonic activity across WA from October 2010 to May 2011. Satellite-derived sea surface temperature measurements recorded anomalies of up to 5°C above long-term averages. Benthic surveys quantified the extent of bleaching at 10 locations across four regions from tropical to temperate waters. Bleaching was recorded in all locations across regions and ranged between 17% (±5.5) in the temperate Perth region, to 95% (±3.5) in the Exmouth Gulf of the tropical Ningaloo region. Coincident with high levels of bleaching, three cyclones passed in close proximity to study locations around the time of peak temperatures. Follow-up surveys revealed spatial heterogeneity in coral cover change with four of ten locations recording significant loss of coral cover. Relative decreases ranged between 22%-83.9% of total coral cover, with the greatest losses in the Exmouth Gulf. CONCLUSIONS/SIGNIFICANCE: The anomalous thermal stress of 2010-11 induced mass bleaching of corals along central and southern WA coral reefs. Significant coral bleaching was observed at multiple locations across the tropical-temperate divide spanning more than 1200 km of coastline. Resultant spatially patchy loss of coral cover under widespread and high levels of bleaching and cyclonic activity, suggests a degree of resilience for WA coral communities. However, the spatial extent of bleaching casts some doubt over hypotheses suggesting that future impacts to coral reefs under forecast warming regimes may in part be mitigated by southern thermal refugia.

Smell, learn and live: the role of chemical alarm cues in predator learning during early life history in a marine fish.

The speed with which individuals can learn to identify and react appropriately to predation threats when transitioning to new life history stages and habitats will influence their survival. This study investigated the role of chemical alarm cues in both anti-predator responses and predator identification during a transitional period in a newly settled coral reef damselfish, Pomacentrus amboinensis. Individuals were tested for changes in seven behavioural traits in response to conspecific and heterospecific skin extracts. Additionally, we tested whether fish could learn to associate a previously novel chemical cue (i.e. simulated predator scent) with danger, after previously being exposed to a paired cue combining the conspecific skin extract with the novel scent. Fish exposed to conspecific skin extracts were found to significantly decreased their feeding rate whilst those exposed to heterospecific and control cues showed no change. Individuals were also able to associate a previously novel scent with danger after only a single previous exposure to the paired conspecific skin extract/novel scent cue. Our results indicate that chemical alarm cues play a large role in both threat detection and learned predator recognition during the early post-settlement period in coral reef fishes.

Habitat associations of juvenile fish at Ningaloo Reef, Western Australia: the importance of coral and algae.

Habitat specificity plays a pivotal role in forming community patterns in coral reef fishes, yet considerable uncertainty remains as to the extent of this selectivity, particularly among newly settled recruits. Here we quantified habitat specificity of juvenile coral reef fish at three ecological levels; algal meadows vs. coral reefs, live vs. dead coral and among different coral morphologies. In total, 6979 individuals from 11 families and 56 species were censused along Ningaloo Reef, Western Australia. Juvenile fishes exhibited divergence in habitat use and specialization among species and at all study scales. Despite the close proximity of coral reef and algal meadows (10's of metres) 25 species were unique to coral reef habitats, and seven to algal meadows. Of the seven unique to algal meadows, several species are known to occupy coral reef habitat as adults, suggesting possible ontogenetic shifts in habitat use. Selectivity between live and dead coral was found to be species-specific. In particular, juvenile scarids were found predominantly on the skeletons of dead coral whereas many damsel and butterfly fishes were closely associated with live coral habitat. Among the coral dependent species, coral morphology played a key role in juvenile distribution. Corymbose corals supported a disproportionate number of coral species and individuals relative to their availability, whereas less complex shapes (i.e. massive & encrusting) were rarely used by juvenile fish. Habitat specialisation by juvenile species of ecological and fisheries importance, for a variety of habitat types, argues strongly for the careful conservation and management of multiple habitat types within marine parks, and indicates that the current emphasis on planning conservation using representative habitat areas is warranted. Furthermore, the close association of many juvenile fish with corals susceptible to climate change related disturbances suggests that identifying and protecting reefs resilient to this should be a conservation priority.